Roles of steroid hormones in oviductal function

Abstract

The oviduct (known as the fallopian tube in humans) is the site for fertilization and pre-implantation embryo development. Female steroid hormones, estrogen and progesterone, are known to modulate the morphology and function of cells in the oviduct. In this review, we focus on the actions of estrogen and progesterone on secretory, ciliated, and muscle cell functions and morphologies during fertilization, pre-implantation embryo development, and embryo transport in humans, laboratory rodents and farm animals. We review some aspects of oviductal anatomy and histology and discuss current assisted reproductive technologies (ARTs) that bypass the oviduct and their effects on embryo quality. Lastly, we review the causes of alterations in secretory, ciliated, and muscle cell functions that could result in embryo transport defects.

Figure 1:

Gross and histological morphologies of human and mouse oviducts. A. Human oviduct. Top panel: a drawing for gross anatomy of the oviduct. Purple and orange layers represent myosalpinx and endosalpinx layers, respectively. Middle and bottom left panels: Hematoxylin and Eosin (H&E) staining of the ampulla and the isthmus regions of the oviduct demonstrating three tissue layers: endosalpinx, myosalpinx, and mesosalpinx. Middle and bottom right panels: Ampulla and isthmus at higher magnification. B. Mouse oviduct. Top panel: gross anatomy of the female reproductive tract including ovaries, oviducts, and the uterus. Middle and bottom left panels: the cross section of the ovary and the whole oviduct indicating three different regions; the infundibulum, the ampulla, and the isthmus. Middle and bottom right panels: Ampulla and isthmus at higher magnification. Ciliated epithelial cells; CC. Non-ciliated (secretory) epithelial cells; non-CC.

Figure 2:

Scanning electron microscopy (SEM) images of the myosalpinx and the inner endosalpinx. A-D. SEM images of the myosalpinx in the uterotubal junction (UTJ) and isthmic regions after tissue maceration techniques (adapted from (Muglia and Motta 2001) with permission with original scale bars shown). A. Barrier-like salpinx in rat UTJ, bar = 25 μm. B. Sphincter-like type a salpinx in ewe UTJ, bar = 5 μm. C. Plexiform arrangement of myosalpinx in the isthmus in C. human (bar = 100 μm) and D. rabbit (bar = 50 μM). E-F. SEM images of inner endosalpinx at the ampulla region including ciliated and non-ciliated (or secretory) epithelial cells from E. human oviduct [×7,810 magnification, modified with permission from (Seki, et al. 1978)] and F. mouse oviduct [×9,000 magnification, modified with permission from (Dirksen and Satir 1972)]. Motile cilia are present at the apical membrane of ciliated cells and microvilli are present on the apical surface of secretory cells.

Figure 3:

Ciliated epithelial cells (CC) are more abundant in the distal part of the oviduct (including infundibulum and ampulla) whereas the secretory epithelial cells (SC) are more prominent in the proximal part including the isthmus. Muscle cell (MC) layer is also thickest in the proximal compared to the distal region of the oviduct (as also seen in the histological analysis in Fig. 1). Lamina propria (LP) represents fibroblasts underneath epithelial cells in the mucosal folds. Zygote, 2-cell, 4- to 8-cell, morula, and blastocyst stage embryo develops within the oviducts before the transport into the uterine cavity.

Figure 4:

Expression of estrogen and progesterone receptor (ESR1 and PGR) proteins in the mouse oviduct at the infundibulum, the ampulla, and the isthmus. Oviducts were randomly collected from female mice at different stages of the estrus cycle. E; Epithelium, S; Stroma, M; Muscle cells.

Figure 5:

Images from light microscopy of epithelial cell layer of oviducts collected from the fimbria region at different days of the menstrual cycle in Rhesus monkeys. Days 2, 5-6, 15, and 27 represent days after menstruation. All images are taken at ×1200 magnification (adapted from (Brenner 1969) with permission).

Figure 6:

Actions of estrogen and progesterone in the oviductal cells in the oviducts. Estrogen and progesterone exhibit different effects on secretory, ciliated, and muscle cells in the oviduct. Estrogen- and progesterone-mediated signals are represented with green and red lines, respectively. The overall summation of estrogen and progesterone action is to increase and decrease the embryo transport rate, respectively, within the oviduct. CBF; ciliary beat frequency.